1887

Abstract

Within their host plants, viruses spread from the initially infected cell through plasmodesmata to neighbouring cells (cell-to-cell movement), until reaching the phloem for rapid invasion of the younger plant parts (long-distance or vascular movement). (CPMV) moves from cell-to-cell as mature virions via tubules constructed of the viral movement protein (MP). The mechanism of vascular movement, however, is not well understood. The characteristics of vascular movement of CPMV in (cowpea) were examined using GFP-expressing recombinant viruses. It was established that CPMV was loaded into both major and minor veins of the inoculated primary leaf, but was unloaded exclusively from major veins, preferably class III, in cowpea trifoliate leaves. Phloem loading and unloading of CPMV was scrutinized at the cellular level in sections of loading and unloading veins. At both loading and unloading sites it was shown that the virus established infection in all vascular cell types with the exception of companion cells (CC) and sieve elements (SE). Furthermore tubular structures, indicative of virion movement, were never found in plasmodesmata connecting phloem parenchyma cells and CC or CC and SE. In cowpea, SE are symplasmically connected only to the CC and these results therefore suggest that CPMV employs a mechanism for phloem loading and unloading that is different from the typical tubule-guided cell-to-cell movement in other cell types.

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2002-06-01
2020-01-22
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References

  1. Bendayan, M. & Zollinger, M. ( 1983; ). Ultrastructural localization of antigenic sites on osmium-fixed tissues applying the protein A–gold technique. Journal of Histochemistry and Cytochemistry 31, 101-109.[CrossRef]
    [Google Scholar]
  2. Blackman, L. M., Boevink, P., Santa Cruz, S., Palukaitis, P. & Oparka, K. J. ( 1998; ). The movement protein of cucumber mosaic virus traffics into sieve elements in minor veins of Nicotiana clevelandii. Plant Cell 10, 525-537.[CrossRef]
    [Google Scholar]
  3. Canto, T. & Palukaitis, P. ( 1999; ). Are tubules generated by the 3a protein necessary for cucumber mosaic virus movement? Molecular Plant–Microbe Interactions 12, 985-993.[CrossRef]
    [Google Scholar]
  4. Carrington, J. C., Kasschau, K. D., Mahajan, S. K. & Schaad, M. C. ( 1996; ). Cell-to-cell and long-distance transport of viruses in plants. Plant Cell 8, 1669-1681.[CrossRef]
    [Google Scholar]
  5. Chapman, S., Kavanagh, T. & Baulcombe, D. ( 1992; ). Potato virus X as a vector for the gene expression in plants. Plant Journal 2, 549-557.
    [Google Scholar]
  6. Cheng, N. H., Su, C. L., Carter, S. A. & Nelson, R. S. ( 2000; ). Vascular invasion routes and systemic accumulation patterns of tobacco mosaic virus in Nicotiana benthamiana. Plant Journal 23, 349-362.[CrossRef]
    [Google Scholar]
  7. D’Arcy, C. J. & Zoeten, G. A. ( 1979; ). Beet western yellows virus in phloem tissue of Thlaspi arvense. Phytopathology 69, 1194-1198.[CrossRef]
    [Google Scholar]
  8. Ding, X. S., Carter, S. A., Deom, C. M. & Nelson, R. S. ( 1998; ). Tobamovirus and potyvirus accumulation in minor veins of inoculated leaves from representatives of Solanaceae and Fabaceae. Plant Physiology 116, 125-136.[CrossRef]
    [Google Scholar]
  9. Esau, K. & Hoefert, L. ( 1972; ). Development of infection with beet western yellows virus in sugarbeet. Virology 48, 724-738.[CrossRef]
    [Google Scholar]
  10. Fisher, D. B. & Cash-Clark, C. E. ( 2000; ). Sieve tube unloading and post-phloem transport of fluorescent tracers and proteins injected into sieve tubes via severed aphid stylets. Plant Physiology 123, 125-137.[CrossRef]
    [Google Scholar]
  11. Foster, R. L. S., Beck, D. L., Guilford, P. J., Voot, D. M., Van Dolleweerd, C. J. & Andersen, M. T. ( 1992; ). The coat protein of white clover mosaic potexvirus has a role in facilitating cell-to-cell transport in plants. Virology 191, 480-484.[CrossRef]
    [Google Scholar]
  12. Gilbertson, R. L. & Lucas, W. J. ( 1996; ). How do viruses traffic on the ‘vascular highway’? Trends in Plant Science 1, 260-268.[CrossRef]
    [Google Scholar]
  13. Goldbach, R. W. & Wellink, J. ( 1996; ). Comoviruses: molecular biology and replication. In The Plant Viruses: Polyhedral Virions and Bipartite RNA Genomes , pp. 35-76. Edited by B. D. Harrison & A. F. Murant. New York:Plenum.
  14. Gopinath, K., Wellink, J., Porta, C., Taylor, K. M., Lomonossoff, G. P. & Van Kammen, A. ( 2000; ). Engineering cowpea mosaic virus RNA-2 into a vector to express heterologous proteins in plants. Virology 267, 159-173.[CrossRef]
    [Google Scholar]
  15. Hibi, T., Rezelman, G. & Van Kammen, A. ( 1975; ). Infection of cowpea mesophyll protoplasts with cowpea mosaic virus. Virology 64, 308-318.[CrossRef]
    [Google Scholar]
  16. Hickey, L. J. ( 1979; ). A revised classification of the architecture of dicotyledonous leaves. In Anatomy of the Dicotyledons , pp. 25-39. Edited by C. R. Metcalf & L. Chalk. New York:Oxford University Press.
  17. Kasteel, D., Wellink, J., Verver, J., Van Lent, J., Goldbach, R. & Van Kammen, A. ( 1993; ). The involvement of cowpea mosaic virus M RNA-encoded proteins in tubule formation. Journal of General Virology 74, 1721-1724.[CrossRef]
    [Google Scholar]
  18. Kempers, R. & Van Bel, A. J. E. ( 1997; ). Symplasmic connections between sieve element and companion cell in the stem phloem of Vicia faba L. have a molecular exclusion limit of at least 10 kDa. Planta 201, 195-201.[CrossRef]
    [Google Scholar]
  19. Kempers, R., Prior, D. A. M., Van Bel, A. J. E. & Oparka, K. J. ( 1993; ). Plasmodesmata between sieve element and companion cell of extrafascicular phloem of Cucurbita maxima permit passage of 3 kDa fluorescent probes. Plant Journal 4, 567-575.[CrossRef]
    [Google Scholar]
  20. Leisner, S. M., Turgeon, R. & Howell, S. H. ( 1992; ). Long distance movement of cauliflower mosaic virus in infected turnip plants. Molecular Plant–Microbe Interactions 5, 41-47.[CrossRef]
    [Google Scholar]
  21. Leisner, S. M., Turgeon, R. & Howell, S. H. ( 1993; ). Effects of host plant development and genetic determinants on the long-distance movement of cauliflower mosaic virus in Arabidopsis. Plant Cell 5, 191-202.[CrossRef]
    [Google Scholar]
  22. Murant, A. F. & Roberts, I. M. ( 1979; ). Virus-like particles in phloem tissue of chervil (Anthriscus cerefolium) infected with carrot red leaf virus. Annals of Applied Biology 92, 343-346.[CrossRef]
    [Google Scholar]
  23. Mutterer, J. D., Stussi-Garaud, C., Michler, P., Richards, K. E., Jonard, G. & Ziegler-Graff, V. ( 1999; ). Role of the beet western yellows virus readthrough protein in virus movement in Nicotiana clevelandii. Journal of General Virology 80, 2771-2778.
    [Google Scholar]
  24. Nelson, R. S. & Van Bel, A. J. E. ( 1998; ). The mystery of virus trafficking into, through and out of vascular tissue. Progress in Botany 59, 476-533.
    [Google Scholar]
  25. Oparka, K. J. & Santa Cruz, S. ( 2000; ). The great escape: phloem transport and unloading of macromolecules. Annual Review of Plant Physiology and Plant Molecular Biology 51, 323-347.[CrossRef]
    [Google Scholar]
  26. Oparka, K. J., Roberts, A. G., Prior, D. A. M. & Santa Cruz, S. ( 1996; ). Viral coat protein is targeted to, but does not gate, plasmodesmata during cell-to-cell movement of potato virus X. Plant Journal 10, 805-813.[CrossRef]
    [Google Scholar]
  27. Perbal, M. C., Thomas, C. L. & Maule, A. J. ( 1993; ). Cauliflower mosaic virus gene I product (P1) forms tubular structures which extend from the surface of infected protoplasts. Virology 195, 281-285.[CrossRef]
    [Google Scholar]
  28. Reynolds, E. S. ( 1963; ). The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology 17, 208-212.[CrossRef]
    [Google Scholar]
  29. Ritzenthaler, C., Schmit, A. C., Michler, P., Stussi-Garaud, C. & Pinck, L. ( 1995; ). Grapevine fanleaf nepovirus P38 putative movement protein is located on tubules in vivo. Molecular Plant–Microbe Interactions 8, 379-387.[CrossRef]
    [Google Scholar]
  30. Roberts, A. G., Santa Cruz, S., Roberts, I. M., Prior, D. A. M. & Turgeon, R. ( 1997; ). Phloem unloading in sink leaves of Nicotiana benthamiana: comparison of a fluorescent solute with a fluorescent virus. Plant Cell 9, 1381-1396.[CrossRef]
    [Google Scholar]
  31. Santa Cruz, S. ( 1999; ). Perspective: phloem transport of viruses and macromolecules – what goes in must come out. Trends in Microbiology 7, 237-241.[CrossRef]
    [Google Scholar]
  32. Séron, K. & Haenni, A. L. ( 1996; ). Vascular movement of plant viruses. Molecular Plant–Microbe Interactions 9, 435-442.[CrossRef]
    [Google Scholar]
  33. Shepardson, S., Esau, K. & McCrum, R. ( 1980; ). Ultrastructure of potato leaf phloem infected with potato leafroll virus. Virology 105, 379-392.[CrossRef]
    [Google Scholar]
  34. Storms, M. M. H., Van der Schoot, C., Prins, M., Kormelink, R., Van Lent, J. W. M. & Goldbach, R. W. ( 1995; ). The nonstructural NSm protein of tomato spotted wilt virus induces tubular structures in plant and insect cells. Virology 214, 485-493.[CrossRef]
    [Google Scholar]
  35. Sudarshana, M. R., Wang, H. L., Lucas, W. J. & Gilbertson, R. L. ( 1998; ). Dynamics of bean dwarf mosaic geminivirus cell-to-cell and long-distance movement in Phaseolus vulgaris revealed, using the green fluorescent protein. Molecular Plant–Microbe Interactions 11, 277-291.[CrossRef]
    [Google Scholar]
  36. Thompson, G. A. & Schulz, A. ( 1999; ). Macromolecular trafficking in the phloem. Trends in Plant Science 4, 354-360.[CrossRef]
    [Google Scholar]
  37. Turgeon, R. ( 2000; ). Plasmodesmata and solute exchange in the phloem. Australian Journal of Plant Physiology 27, 521-529.
    [Google Scholar]
  38. Van Beek, N. A. M., Derksen, A. C. G. & Dijkstra, J. ( 1985; ). Polyethylene glycol-mediated infection of cowpea protoplasts with sonchus yellow net virus. Journal of General Virology 66, 551-557.[CrossRef]
    [Google Scholar]
  39. Van Bel, A. J. E. ( 1996; ). Interaction between sieve element and companion cell and the consequences for photoassimilate distribution. Two structural hardware frames with associated physiological software packages in dicotyledons. Journal of Experimental Botany 47, 1129-1140.[CrossRef]
    [Google Scholar]
  40. Van Bel, A. J. E. & Kempers, R. ( 1997; ). The pore/plasmodesma unit: key element in the interplay between sieve element and the companion cell. Progress in Botany 58, 278-291.
    [Google Scholar]
  41. Van Bokhoven, H., Verver, J., Wellink, J. & Van Kammen, A. ( 1993; ). Protoplasts transiently expressing the 200K coding sequence of cowpea mosaic virus B-RNA support replication of M-RNA. Journal of General Virology 74, 2233-2241.[CrossRef]
    [Google Scholar]
  42. Van Lent, J. W. M. & Verduin, B. J. M. ( 1986; ). Detection of viral protein and particles in thin sections of infected plant tissue using immunogold labelling. In Developments in Applied Biology: Developments and Applications in Virus Testing , pp. 193-211. Edited by R. A. C. Jones & L. Torrance. Wellesbourne:Association of Applied Biologists.
  43. Van Lent, J. W. M. & Verduin, B. J. M. ( 1987; ). Detection of viral antigen in semi-thin sections of plant tissue by immunogold-silver staining and light microscopy. Netherlands Journal of Pathology 93, 261-272.[CrossRef]
    [Google Scholar]
  44. Van Lent, J., Storms, M. & Goldbach, R. ( 1990; ). Evidence for the involvement of 58K and 48K proteins in the intercellular movement of cowpea mosaic virus. Journal of General Virology 71, 219-223.[CrossRef]
    [Google Scholar]
  45. Van Lent, J., Storms, M., Van Der Meer, F., Wellink, J. & Goldbach, R. ( 1991; ). Tubular structures involved in movement of cowpea mosaic virus are also formed in infected protoplasts. Journal of General Virology 72, 2615-2623.[CrossRef]
    [Google Scholar]
  46. Wang, H. L., Gilbertson, R. L. & Lucas, W. J. ( 1996; ). Spatial and temporal distribution of Bean dwarf mosaic geminivirus in Phaseolus vulgaris and Nicotiana benthamiana. Phytopathology 86, 1204-1214.[CrossRef]
    [Google Scholar]
  47. Wellink, J. & Van Kammen, A. B. ( 1989; ). Cell-to-cell transport of cowpea mosaic virus requires both the 58K/48K proteins and the capsid proteins. Journal of General Virology 70, 2219-2286.
    [Google Scholar]
  48. Wellink, J., Jaegle, M. & Goldbach, R. ( 1987a; ). Detection of a novel protein encoded by the bottom-component RNA of cowpea mosaic virus, using antibodies raised against a synthetic peptide. Journal of Virology 61, 236-238.
    [Google Scholar]
  49. Wellink, J., Jaegle, M., Prinz, H., Van Kammen, A. & Goldbach, R. ( 1987b; ). Expression of the middle component RNA of cowpea mosaic virus in vivo. Journal of General Virology 68, 2577-2585.[CrossRef]
    [Google Scholar]
  50. Wieczorek, A. & Sanfaçon, H. ( 1993; ). Characterization and subcellular location of tomato ringspot nepovirus putative movement protein. Virology 194, 734-742.[CrossRef]
    [Google Scholar]
  51. Wisniewski, L. A., Powell, P. A., Nelson, R. S. & Beachy, R. N. ( 1990; ). Local and systemic spread of tobacco mosaic virus in transgenic tobacco. Plant Cell 2, 559-567.[CrossRef]
    [Google Scholar]
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